Abstract
The Cerrado is a savanna formation predominantly located in the central Brazilian plateau; this vegetation is rich in bryophytes. This study analyzes bryophyte diversity, composition and distribution among various Cerrado vegetation types (Gallery Forest, Deciduous For-est, Rupestrian Cerrado and Rupestrian Fields) and substrates in the Área de Proteção Ambiental Morro do Macaco, from municipality of Iporá, Goiás state, in Central-West Bra-zil. The collection was performed in four plots of 20m x 20m, in each vegetation types, from August to December 2010, the data were analyzed with the Shannon-Wiener (H’) and Simpson diversity index and the floristic similarity with UPGMA. We found 37 species, with 28 to Bryophyta and nine to Marchantiophyta. Trichostomum brachydontium Bruch is a new record to the Brazilian Midwest and an endemic species (Archidium oblongifolium Peralta et al.) occurs in the study area. The forested areas were the richest in species number and the substrate most colonized was soil. The results extend the information about the Cerrado bryophytes, increasing the knowledge of their taxonomic diversity and ecology.Keywords: mosses, liverworts, community ecology, Brazilian savanna.
Resumo
O Cerrado é uma formação savânica localizada no platô Central do Brazil, apresentando vegetação rica em briófitas. Este trabalho analisou a diversidade de briófitas através da composição e distribuição de briófitas entre as fitofisionomias de Cerrado (Mata Seca, Mata de Galeria, Cerrado Rupestre e Campo Rupestre) e a colonização de substratos na Área de Proteção Ambiental Morro do Macaco, no município de Iporá, no Estado de Goiás, na região Central do Brasil. As coletas ocorreram no interior de quatro parcelas de 20m x 20m demarcadas em cada formação vegetal nos meses de agosto a dezembro de 2010. Foram analisados os índices de Shannon-Wiener (H’) e Simpson e a similaridade entre as fitofisionomias através da técnica UPGMA. Foram encontradas 37 espécies, 28 da divisão Bryophyta e nove de Marchantiophyta. Trichostomum brachydontium Bruch é registrada pela primeira vez para o Centro-Oeste brasileiro e uma espécie endêmica, Archidium oblongifolium Peralta et al., ocorre na área estudada. As áreas florestadas apresentaram maior riqueza de espécies e o substrato mais colonizado foi solo. Os re-sultados obtidos ampliam as informações sobre a diversidade taxonômica e ecologia das briófitas do Cerrado.Palavras-chave: musgos, hepáticas, ecologia de comunidades, savana brasileira.
Bryophyte diversity in an area of Brazilian Cerrado
in Central-West
Briófitas de área de Cerrado da região Centro-Oeste do Brasil
1 Universidade Estadual de Goiás. Campus Iporá. Av. R2,
Quadra 01, s/n, Jardim Novo Horizonte II, 76200-000, Iporá, GO, Brasil.
2 Instituto de Botânica. Av. Miguel Stéfano, 3687,
04301-012, São Paulo, SP, Brasil.
Alex Batista Moreira Rios
1 alexrios_ipo@yahoo.com.brJhonatan Paulo da
Silva Oliveira
1 jhonatan.biosilva@yahoo.com.brRodrigo Pereira da Silva
1 rodrigo.bio1@hotmail.comJosé Firmino de Oliveira Neto
1 neto.09@hotmail.comLuciana Santos Oliveira
1 lucianasantos.o.bio@hotmail.comDenilson Fernandes Peralta
2 denilsonfp@yahoo.com.brDouglas Henrique Bottura
Maccagnan
1Introduction
The Neotropical region is extremely rich in bryophytes,
congregating around a third of the known species, which
are distributed in the various ecosystems that exist from
Mexico to southeastern Brazil (Hallingbäck and Hodgetts,
2000). However, the actual knowledge about the
composi-tion, structure, distribution and ecology of this group of
plant remains incipient or unknown to several Latin
Amer-ican areas, including the Brazilian Cerrado vegetation
do-main (Câmara and Vital, 2006; Câmara, 2008a).
The Cerrado is a savanna formation predominantly
lo-cated in the central Brazilian plateau. This vegetation is rich
in bryophytes and 433 species have already been recorded
for this region, but comparing its area and the number of
works published with the others Brazilian vegetations, it
re-mains as one of the lesser knowledge about the Bryophyte
species diversity (Câmara and Vital, 2004, 2006; Câmara
and Costa, 2006; Câmara, 2008a; Forzza et al., 2010).
In the last decades the Cerrado vegetation has been reduced
to non-continuous fragments with loss of native species
(Machado et al., 2004; Pivello, 2005; Mittermeier et al.,
2005), and concerning about the bryophyte diversity, the
little knowledge is an impediment for conservation actions
and management of their diversity (Santos, 2006).
The Goiás State is totally included in the Cerrado
do-main But few works were developed in this state and there
is 318 bryophyte species recorded. This information comes
from taxonomical works, such as Gradstein et al. (2005);
Yano and Peralta (2007, 2008); Peralta et al. (2008); Sousa
et al. (2008, 2010); Soares et al. (2011); Pinheiro et al.
(2012); Carvalho et al. (2014); Aquino et al. (2015);
Peral-ta et al. (2015); and CosPeral-ta and PeralPeral-ta (2015).
Considering the degradation level of the savannahs by
human action (Myers et al., 2000; Machado et al., 2004)
and the need of information about the Cerrado bryophytes,
this study aimed to survey the bryophytes in the Área de
Proteção Ambiental Morro do Macaco, in the Municipality
of Iporá, state of Goiás, analyzing their diversity,
composi-tion and distribucomposi-tion between various Cerrado vegetacomposi-tion
types and substrates in the area studied.
Material and methods
Study area
The Área de Proteção Ambiental (APA) Morro do
Macaco (16°25’212”S and 51°02’455’W) has an average
area of 1,000 ha (Gomis, 1998); the altitude ranges from
400 to 800 m.s.l. and belongs to the municipality of Iporá,
the largest city in this state (IBGE, 2010). The
municipal-ity’s climate type is tropical semi-humid (Alves, 2011), with
dry and rainy seasons well defined, where the annual
rain-fall are 1,200 to 1,600 mm (Longhi et al., 2005). The rainrain-fall
season is concentrated during the months of November and
March, with 100 and 300 mm of month mean, this period
also recorded the highest temperatures means above 30°C
(SECTEC/SIMEHGO, 2011). The soils are of the Oxisol
and Red-Yellow with medium texture; the topography is
un-dulating and the vegetation composed by remnants of native
Cerrado (Longhi et al., 2005; Cunha et al., 2007).
The vegetation of the studied area is composed mainly
of Gallery Forest, Deciduous Forest, Rupestrian Cerrado
and Rupestrian Fields, with the forest formations
concen-trated at the base and tip of the hill. This area was chosen
for this survey because after observing the field we
consid-ered it a very preserved remnant, because the soil is hardly
rock and hence very difficult for agriculture and farming.
The Area is a conservation unit of Sustainable Use
(Brasil, 2006) named APA (Environmental Protect Area,
in Portuguese “Área de Proteção Ambiental”) and
estab-lished by the law no. 871, of June 23, 1997 (Iporá, 1997).
Methods
Samples were collected from August to December of
2010 in the following vegetation types: Gallery Forest,
Deciduous Forest, Rupestrian Cerrado and Rupestrian
Fields, in all average substrates. In order to analyze the
composition and distribution of bryophytes in each
vegeta-tion type we collected 16 plots, four plots of 20m x 20m
(400m²) for each vegetation type, with minimum distance
of 100m between them. We used the collection
methodolo-gy for this group described by Wiggers and Stange (2008).
The samples are deposited in the herbaria SP (Herbarium
SP – “Maria Eneyda P. Kauffman Fidalgo) and UEG
(Her-barium UEG – Universidade Estadual de Goiás).
The identifications were done based on Jovet-Ast
(1991), Sharp et al. (1994), Buck (1998), Gradstein and
Costa (2003), Bordin and Yano (2013), as well as the
clas-sification system by Goffinet et al. (2009) for the
Bryo-phyta and Crandall-Stotler et al. (2009) for
Marchantio-phyta. The samples were also classified according to the
substrate from which they were extracted, as follows: soil,
bark, litter, and rock, according Robins (1952).
Diversity analyzes of Shannon-Wiener (H’) and
Simp-son indexes was calculated with the Statistica 7.0 software.
The UPGMA cluster analysis among the vegetation types
was calculated using the usind the presence/absence of the
species. The distances were calculated by Pearson index
(Legendre and Legendre, 1998).
Results and discussion
348 samples and found 37 bryophyte species (Table 1),
with 28 species of Bryophyta in 20 genera and 16 families
were analyzed. The most represented families are
Fissi-dentaceae (seven species) and Pottiaceae (four species).
The samples were collected during the end of the dry
sea-son and the beginning of the rainy seasea-son, factors that
in-fluenced the low occurrence of sporophytes, as described
by Castro et al. (2002).
Trichostomum brachydontium Bruch.(Pottiaceae) is
described in the literature as occurring from Mexico to
Brazil (Sharp et al., 1994), but in Brazil it is recorded only
to the Northeast and Southeast (Forzza et al., 2010). This
new record is an important fill of the gap in the Mid-West,
and encourages the development of new researches in this
region, as commented by Câmara and Vital (2004).
The samples collected for this survey were used to
describe Archidium oblongifolium Peralta et al.
(Archi-diaceae, subg. Archidiella). This species is recognized as
Taxa GF DF RC RF SO BA RO LI Voucher
Pseudosymblepharis schimperiana (Paris) H.A.Crum 3 22 56 19 100 - - - Cunha 7
Helicophyllum torquatum (Hook.) Brid. 14 86 - - - 36 57 7 Silva 21
Entodontopsis leucostega (Brid.) W.R.Buck & Ireland 16 69 13 2 14 32 26 28 Rios 32
Fissidens goyazensis Broth. 17 50 33 - 100 - - - Rios 153
Archilejeunea parviflora (Nees) Schiffn. 20 80 - - - 70 20 10 Silva 23
Hyophilla involuta (Hook.) A.Jaeger 25 75 - - - 25 75 - Rios 77
Eulacophyllum cultelliforme (Sull.) W.R.Buck & Ireland 95 - 5 - 42 5 53 - Oliveira-Neto 34
Fissidens pallidinervis Mitt. 100 - - - 66 17 - 17 Rios 157
Cyathodium cavernarum Kunze 100 - - - 67 - 33 - Rios 148
Fissidens angustifolius Sull. 100 - - - 100 - - - Rios 149
Fissidens flaccidus Mitt. 100 - - - 100 - - - Rios 160
Fissidens lindbergii Mitt. 100 - - - 100 - - - Rios 150
Fissidens zollingeri Mont. 100 - - - 100 - - - Nascimento 6
Fabronia macroblepharis Schwägr. 100 - - - - 100 - - Rios 115
Fissidens pellucidus Hornsch. 100 - - - 100 - Rios 161
Macromitrium carionis Müll. Hal. 100 - - - 100 - Rios 68
Frullania gibbosa Nees - 60 40 - 40 20 40 - Rios 38
Frullania dusenii Steph. - 89 11 - - 56 22 22 Rios 30
Acrolejeunea emergens (Mitt.) Steph. - 100 - - - 40 40 20 Rios 52
Erpodium coronatum (Hook. & Wilson) Mitt. - 100 - - - 50 - 50 J.Oliveira 35
Fabronia ciliaris (Brid.) Brid. - 100 - - - 100 - - Silva 15
Ochrobryum subulatum Hampe - 100 - - - 100 - - Rios 39
Octoblepharum albidum Hedw. - 100 - - - 100 - - Rios 39
Acrolejeunea torulosa (Lehm. & Lindenb.) Schiffn. - 100 - - - - 100 - Silva 17
Trichostomum brachydontium Bruch - - 12 88 100 - - - Rios 93
Archidium oblongifolium Peralta et al. - - 25 75 100 - - - Rios 110
Weissia controversa Hedw. - - 33 67 100 - - - Rios 101
Riccia wainionis Steph. - - 50 50 100 - - - L.Oliveira 36
Erythrodontium longisetum (Hook.) Paris - - 100 - - 100 - - Rios 3
Archidium ohioense Schimp. ex Müll. Hal. - - - 100 100 - - - Rios 20
Bryum apiculatum Schwägr. - - - 100 100 - - - Rios 83
Chryso-hypnum diminutivum (Hampe) W.R.Buck * - - - Rios 37
Lopholejeunea nigricans (Lindenb.) Schiffn * - - - Rios 34
Mastigolejeunea auriculata (Wilson) Schiffn. * - - - Rios 77
Ochrobryum gardneri (Müll.Hal.) Lindb. * - - - Rios 35
Tisserantiella minutissima (Mitt.) R.H.Zander* - - - Rios 49
Trachyphyllum dusenii (Müll.Hal. ex Broth.) Broth. * - - - Silva 25
Table 1. Species list and distribution with relative frequency (%) by vegetation types and substrates in the APA Morro do Macaco, Iporá
endemic of the rupestrian Cerrado and Rupestrian Fields
of the APA Morro do Macaco (Peralta et al., 2015).
Entodontopsis leucostega (Brid.) W.R. Buck &
Ire-land (Stereophyllaceae) was the most frequent species,
with occurrence in 163 (47%) of the samples analyzed.
This moss has wide Neotropical range and is commonly
recorded in the works performed in the Cerrado by Sharp
et al. (1994); Câmara and Leite (2005); Carvalho et al.
(2014); and Aquino et al. (2015).
For the liverworts we found nine species in seven
gen-era and four families. The Lejeuneaceae was the richest
family, with five species, followed by Frullaniaceae, with
two species. Similarly, in other inventories in Neotropical
areas, Lejeunaceae has been recorded as the richest family
of liverworts and sometimes has nearly more than 50% of
the liverworts species, as listed by Peralta and Yano (2005)
for a swamp area in the Cerrado region; and Valente and
Pôrto (2006) and Campelo and Pôrto (2007) for remnants
of Atlantic Forest.
Vilas Bôas-Bastos and Bastos (1998) related the great
occurrence of leaf liverworts, such as Lejeuneaceae and
Frullaniaceae, with xerophytic condition that allow the
development of species of large ecological amplitude
tol-erant of solar radiation exposition. Similar results were
found in the APA Morro do Macaco.
The species recorded comprise 8% of the bryophyte
species recorded to the Cerrado region and 13% of the
Goiás State (Costa and Peralta, 2015).
Localities Species number Common species with APA
Municipality of Alagoinhas, BA (Vilas Bôas-Bastos e Bastos, 1998). 27 4
Jalapão, TO (Câmara e Leite, 2005). 22 4
Parque Estadual da Serra dos Pireneus and proximitys, GO (Sousa et al., 2008). 58 3
Reserva do IBGE, RECOR, DF (Câmara, 2008a). 26 5
Reserva do IBGE, RECOR, DF (Câmara, 2008b). 15 1
Parque Estadual da Serra dos Pireneus, GO (Sousa et al., 2010). 68 10
Parque Nacional de Brasília, DF (Soares et al., 2011) 55 6
Parque Nacional das Chapadas dos Veadeiros, GO (Pinheiro et al., 2012) 36 1
Serra de Caldas Novas, GO (Carvalho et al., 2014). 36
7
Municipality of Quirinópolis, GO (Aquino et al., 2015). 38
6
Table 2. Comparison among the floristic list of APA Morro do Macaco (37 species), Iporá municipality, Goiás, Central-western Brazil and
the published data of Cerrado vegetation works.
Figure 1. Bryophyte species by vegetation types in APA Morro do Macaco, Iporá municipality, Goiás, Central-western Brazil. Black: total
For richness comparation we discharge the sampling
effort, once the work published used for comparation
do not describe in details the collection methods. The
works performed in the Cerrado region developed by
Vilas Bôas-Bastos and Bastos (1998) recorded 23
spe-cies; Câmara and Leite, with 22 species (2005); Sousa
et al. (2008), with 58 species; Câmara (2008a) with 26
species; Câmara (2008b), with 15 species; Sousa et al.
(2010), with 68 species; Soares et al. (2011), with 55
spe-cies; Pinheiro et al. (2012), with 36 spespe-cies; Carvalho
et al. (2014), with 36 species and, Aquino et al. (2015),
with 38 species. According to Pinheiro et al. (2012) and
Peralta et al. (2015), the micro-habitat heterogeneity
pro-vide specific conditions of soil texture and composition
and humidity essential for the establishment of the
bryo-phytes, and the existent conditions in the APA, including
forested areas and gross rock, constitute a wide gradient
for bryophytes.
The Gallery Forest was the vegetation type with the
highest species richness (S=16, nine of them exclusive),
followed by dry forest (S=14, six exclusive), Rupestrian
Cerrado (S=11 species) and Rupestrian Field (S=8, two
exclusive) (Table 2, Figure 1). The highest diversity
indi-ces were found in the Gallery Forest and Dry Forest, while
the highest values for the Simpson index were obtained for
the formations Rupestrian Cerrado and Rupestrian Field
(Table 3). These results follow the discussion provided by
Vilas Bôas-Bastos and Bastos (1998); Sousa et al. (2010);
and Aquino et al. (2015) relating the forested areas with
greater water availability and few dry exposed areas.
Our cluster analyses of the bryophyte distribution
among the vegetation types found in APA Morro do
Maca-co show three groups: (i) Dry Forest and Rupestrian
Cer-rado, (ii) Gallery Forest, (iii) Rupestrian Field (Figure 2).
The Rupestrian Cerrado compared to Rupestrian Field
of-fers greater variety of habitats, especially the occurrence
of trunks, for colonization by mosses and liverworts, a
fac-tor that probably makes this vegetation type closer to Dry
Forest. Visnadi (2004) found differences between species
composition in grassland and savanna formations in the
Reserva Biológica e Estação Experimental Mogi-Guaçu,
in São Paulo state.
Considering only the mosses, the cluster topology of
the vegetation types did not change the distribution pattern
(Figure 3). However, to the liverworts, the topology has
changed (Figure 4) for only two groups: (i) Forest
tions of Gallery and Dry Forest; and (ii) Rupestrian
forma-Vegetation types H’ D
Gallery Forest 2.328 0.139
Dry Forest 2.005 0.220
Rupestrian Cerrado 1.740 0.276
Rupestrian Field 1.436 0.356
Table 3. Shannon-Wiener (H’) and Simpson (D) index from four
vegetation types in APA Morro do Macaco (November – Dezember 2010), Iporá municipality, Goiás, Central-western Brazil.
Figure 2. Vegetation types cluster by Pearson index and UPGMA, including all species found in APA Morro do Macaco, Iporá municipality,
tions of Cerrado and Field. Santos et al. (2011) described
the distribution of the bryophytes in forested areas of
At-lantic Forest vegetation types as related to the stable
micro-climate that differ from the open vegetation. Carvalho et
al. (2014) described the open vegetation as a barrier of dry
intolerant species, similarly to our observations in the APA,
because in the greatest elevations the Rupestrian is not
colonized by the forest species, even with a small distance.
The cluster analysis indicate that Bryophyta is better
than Marchantiophytae to group the forested areas of
Gal-Figure 3. Vegetation type cluster by Pearson index and UPGMA, including only mosses found in APA Morro do Macaco, Iporá
municipal-ity, Goiás, Central-western Brazil.
Figure 4. Vegetation type cluster by Pearson index and UPGMA, including only liverworts found in APA Morro do Macaco, Iporá
lery Forest with Deciduous Forest and the open exposed
areas of Rupestrian Cerrado with Rupestrian Fields,
con-trasting with the results of Visnadi (2004), in the Cerrado of
Mogi Guaçu, in which liverworts is a group that established
greater similarity between the vegetation types studied.
The colonization of the substrate predominance are in
the following ascending order: soil (17 species); rocky
sur-faces (12 species), and bark (15 species) (Table 2, Figure 5).
The occurrence on soil and rock of 65% of the species
in the APA characterizes the area as stable and indicates
specialization in the substrate colonization. These results
differ from other studies in the country, in which the most
colonized substrate was bark (Molinaro and Costa, 2001;
Ilkiu-Borges et al., 2004; Valente et al., 2009). In an
evalu-ation of the all species of the Cerrado, Costa and Peralta
(2015) also describe bark and soil as the most common
substrates colonized. According to Santos et al. (2011) and
Carvalho et al. (2014), the vegetation acts as filters on the
expansion of the communities on the ecosystems.
Our results indicate that the APA Morro do Macaco is
an important remnant of Cerrado for bryophytes, since 37
species were found, with one new citation to the Mid-West
region and an endemic species. The forested areas were
the richest in species number and the substrate most
colo-nized was soil.
Considering the degradation process of the Cerrado
vegetation, our results encourage new surveys in this
eco-system in order to fill distribution gaps and ecological
characterization of the communities, as well as to
contrib-ute for future APA conservation acts.
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